A selective trade-off between mimicry and hybridization in woodpeckers

The story behind our recent paper.

Don’t be afraid to explore crazy ideas. That is the lesson I learned from my latest publication in the Journal of Avian Biology. In this blog post, I will not only share the main results of this paper, but also the entire process behind the scenes. A nice example that the development of a paper is rarely linear.

Woodpecker Hybrids

It all started with my quest to assess the reliability of hybrid records in birds. Generally, the reliability of these records has been taken at face value. However, detailed assessments of certain hybrids in the Handbook of Avian Hybrids of the World and the Serge Dumont Bird Hybrids Database revealed that some cases are unreliable or incorrect. For example, only one out of four records of tinamou hybrids turned out to be supported by convincing evidence (see this paper for the details). That is why I decided to revisit hybrids records in several bird groups. The next group on the list were the woodpeckers. There was no particular reason for this choice. Woodpeckers are just very cool birds.

My exploration of old papers and handbooks uncovered 68 hybrid combinations of which 37 cases (54.41%) were supported by convincing evidence. In total, 88 species (36.67%) were reported to have hybridized with at least one other species. However, only 46 species (19.17%) had reliable hybrid records. These numbers indicate that many hybrid records will need to be re-evaluated. I have described an example of an unreliable case in another blog post. A putative hybrid between Chestnut-colored Woodpecker (Celeus castaneus) and Golden-olive Woodpecker (Piculus rubiginosus) could be traced back to an erroneous interpretation of a footnote in a checklist of Mexican birds. Always check the original source.

Enter Mimicry

Now what? This question popped into my head when I had finished my list of reliable woodpecker hybrids. I could publish this overview in a short paper, but I wanted to add something. Then I remembered a blog post that I wrote some time ago: “Why do Robust Woodpecker, Lineated Woodpecker and Helmeted Woodpecker look alike?” These three species belong to different genera, but look scarily similar. This impressive case of plumage convergence can be explained by the “interspecific social dominance hypothesis” which states that subordinate species will look like a dominant one to avoid attacks by the dominant species.

This phenomenon got me thinking about the relationship between hybridization and mimicry. During a quick literature search, I discovered a paper by David Pfennig and David Kikuchi in which they discuss several mechanisms that can hamper the evolution of mimicry. One interesting possibility concerns the “selective trade-off hypothesis” where opposing selective forces prevent the evolution of perfect mimicry. Looking at the relationship between hybridization and mimicry suggested a potential trade-off: selection for mimicry drives plumage convergence whereas selection against maladaptive hybridization leads to plumage divergence.

From left to right: Robust Woodpecker (Campephilus robustus), Lineated Woodpecker (Dryocopus lineatus) and Helmeted Woodpecker (Celeus galeatus). From: Fernández et al. (2020).

Tipping Point

To analyze the relationship between hybridization and mimicry, I collected data on mimicry complexes in woodpeckers. Next, for one of these analyses, I needed to know which woodpecker species occur in the same area. I reached out on Twitter and Michaël Nicolaï volunteered to help out. I send him my list of woodpecker species, and he provided me with an overview of sympatric species. My first Twitter-collaboration!

The analyses revealed a clear pattern. We found a clear tipping point in the probability of hybridization and mimicry at ca. 9 million years of divergence. Around this timepoint, the probability of hybridization approaches zero while the probability of belonging to a mimicry complex increases. It looked almost too good to be true. However, we highlighted that this finding is only correlational and remains to be confirmed in other taxonomic groups. We would expect different tipping points in different bird groups (depending on the timepoint when the probability of hybridization reaches zero). Nonetheless, our results suggest a selective tradeoff between evolving interspecific mimicry and avoiding maladaptive hybridization in woodpeckers.

A crazy idea that culminated in an exciting paper.

The relationship between the incidence of hybridization (pink) and the evolution of mimicry complexes (blue) in woodpeckers. (A) Binary logistic regressions show an inverse relationship between hybridization and mimicry complexes, with a tipping point around nine million years of divergence. (B) The distribution of divergence times shows little overlap between hybridizing species and mimicry complexes. From: Ottenburghs & Nicolaï (2024).

References

Ottenburghs, J., & Nicolaï, M. P. (2024). Hybridization constrains the evolution of mimicry complexes in woodpeckers. Journal of Avian Biology, e03228.

Featured image: Downy woodpecker (Dryobates pubescens) © Rhododendrites | Wikimedia Commons

Picky Woodpeckers: Nest selection of Great Spotted Woodpeckers in Italy

These woodpeckers prefer big trees with plenty of food in the surroundings.

The Great Spotted Woodpecker (Dendrocopos major) is the most abundant woodpecker species in Europe. Although this large species is a generalist, it does seem to have a preference for certain habitat types. In a recent paper, Elena Piacentini and Gianpasquale Chiatante investigated habitat and nest selection of Great Spotted Woodpeckers in the Italian region Lombardy. They encountered these birds in human-dominated habitats, such as reforestations and poplar plantations, as well as natural woodlands. When it concerned nest selection, however, the Great Spotted Woodpecker showed a clear preference.

Saproxylic Beetles

During the 2021 breeding season, the researchers discovered 19 nests, which were all located in the woodland areas. Detailed analyses of the forest characteristics around the nest revealed several key features.

[N]esting plots, compared to random plots, have a greater number of trees, which are characterized by a greater presence of holes created by saproxylic beetles and with an average DBH [i.e. diameter at breast height] greater than 18 cm.

These findings suggest that Great Spotted Woodpeckers choose their nesting sites in relation to food availability. In addition, the preference for bigger trees has been reported in other studies (e.g., in Poland and Hungary) and can probably be explained by their suitability to excavate a nest.

The probability of a woodpecker nest increases with the amount of beetle holes per tree. From: Piacentini & Chiatante (2022).

Non-native Trees

Most nests – 11 out of 19 – were found in White Poplar (Populus alba). Interestingly, the Great Spotted Woodpeckers also nested in non-native trees, such as Black Locust (Robinia pseudoacacia). These observations highlight the generalist and adaptive nature of the Great Spotted Woodpecker. As long as the tree is big enough, they will consider them for nesting. While conservationists might worry about the spread of non-native species, the woodpeckers don’t care and just carry on with their lives.

A Personal Note

You might be wondering why I wrote a blog post about nest selection of Great Spotted Woodpeckers, even though this website focuses on avian hybridization. The reason is simple. Recently, I have started a research project into habitat and nest selection of woodpeckers in a Dutch forest. Last spring, a MSc student compared the forest characteristics around 16 Great Spotted Woodpecker nests. This year, another MSc student will continue this survey. To keep up to date with the latest developments, I dove into the literature on woodpecker habitat and nest selection. And the best way to learn about a new topic is to write about it. I hope you enjoyed it.

References

Piacentini, E., & Chiatante, G. (2022). Habitat selection, density and breeding of Great Spotted Woodpecker Dendrocopos major in a protected natural area in northern Italy. Avocetta, 46(2): 97-114.

Featured image: Great Spotted Woodpecker (Dendrocopos major) © Caroline Legg | Wikimedia Commons

Extensive introgression between Red-naped and Yellow-bellied Sapsucker

Genomic analyses uncover many advanced generation hybrids.

In 1952, Thomas Howell published an extensive monograph on the Yellow-Bellied Sapsucker (Sphyrapicus varius) which then comprised four subspecies: varius, nuchalis, daggetti, and ruber. Based on extensive field observations, he attempted to figure out how often these subspecies hybridize. He came to the following conclusions:

Interbreeding between the races where their ranges meet is variable. It is apparently free between ruber and daggetti, moderate between daggetti and nuchalis and between varius and nuchalis, and rare or absent between ruber and nuchalis and between ruber and varius.

In other words, all subspecies seem to interbreed with one another (albeit at different frequencies). Over time, the taxonomy of these woodpeckers has changed. Ornithologists now recognize three distinct species:

• Yellow-Bellied Sapsucker (S. varius)
• Red-naped Sapsucker (S. nuchalis)
• Red-breasted Sapsucker (S. ruber, with subspecies ruber and daggetti)

These classificatory changes have provided some clarity, but the three species still interbreed in several hybrid zones. While these woodpeckers might give taxonomists a headache, they provide exciting opportunities for evolutionary biologists. Previous studies have already described genetic patterns in the hybrid zones between Red-naped and Red-Breasted Sapsucker, and between Red-breasted and Yellow-bellied Sapsucker. The third combination – Red-naped and Yellow-bellied Sapsucker – remained to be characterized with genetic data. Luckily, a recent study in the Journal of Avian Biology filled this knowledge gap.

Hybrid Triangle

Howell (1952) reported moderate hybridization between Red-naped and Yellow-bellied Sapsucker. Is this also reflected in the genetic make-up of these species? Using a set of three traditional markers and a more extensive genomic dataset, Libby Natola and her colleagues explored hybridization dynamics in the Rocky Mountains. The analyses revealed that most birds within the hybrid zone were genetically admixed: 89% based on traditional markers and 52% based on the genomic data. These patterns highlight that traditional markers, such as nuclear genes or microsatellites, tend to overestimate hybridization rates (see also this study on Chukar and Red-legged Partridge). Genomic data provide a more reliable picture.

Next, the researchers performed a more detailed analysis of the admixed individuals. They used “hybrid triangles” to determine the frequency of first-generation hybrids and backcrosses in the hybrid zone. These triangles combine information from a hybrid index (i.e. genetic ancestry of an individual) and the level of heterozygosity to discriminate between different hybrid classes. In general, “pure” individuals are located in the lower corners, while first generation hybrids are at the top. The sides of the triangles indicate backcrosses. These analyses suggested that “the majority of admixed individuals appear to be advanced generation hybrids.”

The “hybrid triangle” shows that most individuals are located on the sides, suggesting that the hybrid zone is comprised of many backcrosses. From: Natola et al. (2021).

Problems with Plumage

Interestingly, the genetic ancestry of these birds was not reflected in their morphology. The researchers used an extensive eight-point system to classify the sapsuckers into different phenotypic classes. However, nineteen birds had genetic ancestry values that did not follow the phenotypic classification. Plumage is thus not a reliable indicator to discriminate between “pure” individuals and several hybrid classes.

And the situation is even more complex than described here. While writing this blog post, another paper on these sapsuckers was published in the journal Molecular Ecology. Apparently, two hybrid zones have collided into a tri-species hybrid zone where all three species interact. The researchers reported that “Surveys of the area […] show that all three species are sympatric, and Genotyping-by-Sequencing identifies hybrids from each species pair and birds with ancestry from all three species.” I will try to cover this study in due time. Stay tuned for another layer of complexity!

References

Billerman, S. M., Cicero, C., Bowie, R. C., & Carling, M. D. (2019). Phenotypic and genetic introgression across a moving woodpecker hybrid zone. Molecular Ecology, 28:1692-1708.

Grossen, C., Seneviratne, S. S., Croll, D. & Irwin, D. E. (2016). Strong reproductive isolation and narrow genomic tracts of differentiation among three woodpecker species in secondary contact. Molecular Ecology 25:4247-4266.

Natola, L., Curtis, A., Hudon, J., & Burg, T. M. (2021). Introgression between Sphyrapicus nuchalis and S. varius sapsuckers in a hybrid zone in west‐central Alberta. Journal of Avian Biology, 52(8).

Natola, L., Seneviratne, S. S., & Irwin, D. (2022). Population genomics of an emergent tri‐species hybrid zone. Molecular Ecology.

Featured image: Red-naped Sapsucker (S. nuchalis) © Matt MacGillivray | Wikimedia Commons

Do Chestnut-colored Woodpecker and Golden-olive Woodpecker hybridize?

A short detective story on the reliability of this peculiar cross.

At the moment, I am exploring the wonderful world of woodpecker hybrids. Checking the Handbook of Avian Hybrids of the World by Eugene McCarthy, I came across a peculiar record: Chestnut-colored Woodpecker (Celeus castaneus) x Golden-olive Woodpecker (Piculus rubiginosus). These species look quite different and diverged more than 11 million years. Never say never when it comes to hybridization in birds, but I was skeptical about this cross. The explanation in the Handbook refers to Miller et al. (1957) who note “an old paper reports a hybrid from Atoyac.” So, I decided to retrace this old paper and verify its reliability.

Do these morphologically distinct species hybridize or not?

Footnote

The study by Miller et al. (1957) turned out to be a checklist of Mexican birds. Below the record of Celeus castaneus, I noticed a footnote that refers to the subspecies Piculus rubiginosus yucatanensis. Although the footnote is located beneath Celeus castaneus, it has nothing to do with this species. So, I assume that McCarthy accidently linked the footnote to Celeus castaneus and inferred a possible hybrid with Piculus rubiginosus. Hence, not a reliable record.

The record of Celeus castaneus and an unrelated footnote that belongs to Piculus rubiginosus.

Original Sources

This ornithological detective story highlights the importance of checking the reliability of bird hybrids. Always return to the original source and assess the evidence directly. In this case, it turned out that McCarthy probably made a mistake while reading the report by Miller and colleagues. When preparing a manuscript in tinamou hybrids, I also noticed that several hybrid records were based on anecdotes and speculation about potential interbreeding. Hardly convincing evidence. That is why it is always a good idea to read the original source when assessing the reliability of avian hybrids.

References

McCarthy, E. M. (2006). Handbook of Avian Hybrids of the World. Oxford university press.

Miller, A. H., Friedmann, H., Griscom, L., & Moore, R. T. (1957). Distributional check-list of the birds of Mexico. Part II. Pacific Coast Avifauna, 33(1), 435.

Featured image: Golden-olive Woodpecker (Piculus rubiginosus) © Gary L. Clark | Wikimedia Commons

Pinpointing “plumage genes” with hybrids between the Yellow-shafted and Red-shafted Flicker

Researchers unravel the genetic basis of particular plumage patches.

Finding the genetic basis of plumage coloration remains one of the most exciting topics in ornithology. In the past, researchers mainly focused on the genes underlying whole-body coloration, such as the white and blue morphs in Snow Geese (Anser caerulescens). Nowadays, we can zoom in on particular patches on the body and use genomic data to pinpoint candidate genes associated with certain plumage patterns. For example, a recent study on Setophaga warblers found that a single genetic variant determined the colors of the cheek, crown and flank in these birds. This study took advantage of hybrids between Townsend’s Warbler (S. townsendi) and Hermit Warbler (S. occidentalis) which show a range of plumage combinations, making it easier to link particular genomic regions to plumage traits.

Another recent study in the Proceedings of the Royal Society B took a similar approach to detect “plumage genes” in the Yellow-shafted Flicker (Colaptes auratus auratus) and the Red-shafted Flicker (C. a. lathami), two woodpeckers differ in the coloration of several plumage patches. Extensive hybridization in North America has resulted in the full range of possible plumage combinations. Stephanie Aguillon and her colleagues used this phenotypic variation to their advantage to find the genes associated with these plumage patches.

Pigments

Before delving into the genomic analyses, we need to understand the difference between two pigments: melanin and carotenoids. The pigment melanin is produced endogenously (i.e. by the bird itself) and leads to grey, black and brown colors. Carotenoids, on the other hand, are obtained through the diet and underlie red, yellow and orange coloration. The plumage patches in the woodpeckers are determined by both pigments types.

The researchers compared the genomes of 10 Yellow-shafted Flickers, 10 Red-shafted Flickers and 48 hybrids. A genome-wide association (GWA) analysis uncovered several genomic regions associated with the plumage patches. Some genomic regions were connected with multiple traits, whereas others were unique to one particular trait. In total, the researchers identified 112 candidate genes.

An overview of the different plumage patches under investigation (figure a). The researchers took advantage of the full range of phenotypes (figure b-c) to identify genomic regions associated with the coloration of these plumage patches (figure d). From: Aguillon et al. (2021).

Candidate Gene CYP2J19

I will not discuss all 112 candidate genes in detail, but focus on one particularly interesting gene: CYP2J19. This gene resides on chromosome 8 and was significantly associated with the coloration of the wing and tail (which form the characteristic shaft). Loyal readers of this blog might recognize the name of this gene: it also underlies the forecrown coloration in Red-fronted Tinkerbird (Pogoniulus pusillus) and Yellow-fronted Tinkerbird (P. chrysoconus), which I covered in a previous blog post. This gene seems to be one of the most important genes determining red and yellow coloration in birds.

The analyses revealed some connections between carotenoid traits and melanin genes. This is very unexpected as these pigments derive from different biochemical pathways. The researchers offer three possible explanations for this surprising finding:

1. The melanin genes have pleiotropic effects, meaning that they affect more than one trait. The regulatory genes associated with melanin production might also control the synthesis of carotenoids.
2. The coloration of some traits is a combination of both pigment types. For example, Yellow-shafted Flickers overlay carotenoids with melanin to produce a black malar stripe.
3. The melanin genes control the absence of melanin within the feathers. A reduction of this pigment will bring out the red or yellow colors.

More detailed genomic analyses are needed to discriminate between these explanations. Luckily, there are plenty of hybrids to work with.

References

Aguillon, S. M., Walsh, J., & Lovette, I. J. (2021). Extensive hybridization reveals multiple coloration genes underlying a complex plumage phenotype. Proceedings of the Royal Society B, 288(1943), 20201805.

Featured image: Red-shafted Northern Flicker (Colaptes auratus lathami) © Dominic Sherony | Wikimedia Commons

From Sweden to Japan: A genetic look at the White-backed Woodpecker

A recent study uncovers four genetic lineages in this widespread species.

During my postdoc in Sweden, I visited the Färnebofjärden National Park, hoping to catch a glimpse of the elusive White-backed Woodpecker (Dendrocopos leucotos). This large woodpecker has a wide distribution, stretching from western Europe to Japan. It has been divided into a dozen morphological subspecies. One of these subspecies – the Amami Woodpecker (owstoni) – is sometimes treated as a separate species, based on its dark plumage. However, morphology is just one aspect in the classification of (sub)species. Are these subspecies also genetically distinct? A recent study in the journal Zoologica Scripta attempted to answer this question by sequencing the DNA of 70 individuals across the range of the White-backed Woodpecker.

Distribution of the White-backed Woodpecker. Colored dots represent sampling locations of different subspecies. From: Pons et al. (2021) Zoologica Scripta.

Four Lineages

The genetic analyses – using three nuclear genes and the mitochondrial gene COI – revealed four distinct lineages. The first split in the evolutionary history of the White-backed Woodpecker occurred about 0.8 million years ago and gave rise to a Chinese lineage that contains two subspecies (tangi and insularis). A third subspecies that was not sampled in this study (fokhiensis) likely belongs to this group. The second split (ca. 0.5 million years ago) separated a southern group (represented by the subspecies lilfordi) from a northern cluster. Later on, this northern cluster was subdivided into a Eurasian (leucotos and uralensis) and a Japanese lineage (namiyei, subcirris, stejnegeri and owstoni). These patterns reveal that the Amami Woodpecker (owstoni) is not genetically differentiated from the other three Japanese subspecies, questioning its species status.

A haplotype network illustrating the four main lineages within the White-backed Woodpecker. From: Pons et al. (2021) Zoologica Scripta.

Genetic Diversity

I can imagine that this bombardment of Latin names can be confusing. So, let’s take a step back and look at the genetic patterns in some of these lineages. In the haplotype network above, you can see one line connecting the Japanese group (in yellow) with the Northern Eurasian lineage. This suggests that Japan was colonized only once by the White-backed Woodpecker, after which it diverged into the different subspecies. On the Eurasian mainland, there is one main haplotype (the big circle in the middle) that can found in Russia and Mongolia. Low genetic diversity across a large range points to a recent population expansion. Most likely, the Eurasian populations can be traced back to a glacial refugium. In contrast, the southern lineage (lilfordi) shows higher levels of genetic diversity. The researchers attribute this pattern to the fragmented distribution of these birds where each mountain population (Pyrenees, Abruzzi and Caucasia) has its own private haplotype. These findings do not only provide more insights into the evolutionary history of the White-backed Woodpecker, but can also guide conservation efforts to preserve high levels of genetic diversity.

References

Pons, J. M., Campión, D., Chiozzi, G., Ettwein, A., Grangé, J. L., Kajtoch, Ł., Mazgajski, T. D., Rakovic, M., Winkler, H. & Fuchs, J. (2021). Phylogeography of a widespread Palaearctic forest bird species: The White‐backed Woodpecker (Aves, Picidae). Zoologica Scripta, 50(2), 155-172.

Featured image: White-backed Woodpecker (Dendrocopos leucotos) © Tokumi | Wikimedia Commons

Why do Robust Woodpecker, Lineated Woodpecker and Helmeted Woodpecker look alike?

Could the interspecific social dominance hypothesis explain this plumage convergence?

I recently bought “All the Birds of the World” from Lynx Editions. The title of the book nicely captures its contents, this huge tome contains beautiful drawings of literally all the (known) bird species in the world. Apart from looking up specific species, I enjoy browsing through the pages and admiring the amazing diversity of birds. Skimming the section on woodpeckers (family Picidae), I noticed the striking similarities between distantly related species. For example, several species seem to have converged upon a plumage pattern that consists of a black-and-white body with an eye-catching red crest. Many ornithologists have made this observation (technically known as mimicry complexes) and there are countless hypotheses to explain why certain woodpecker species look alike.

One possible explanation for this plumage convergence is the “interspecific social dominance hypothesis” which states that subordinate species will look like a dominant one to avoid attacks by the dominant species. A recent study in the Journal of Ornithology tested this hypothesis for three South American woodpeckers.

Niche Differentiation

Juan Manuel Fernández and his colleagues studied the ecology of Robust Woodpecker (Campephilus robustus), Lineated Woodpecker (Dryocopus lineatus) and Helmeted Woodpecker (Celeus galeatus) in Argentina. Based on the size of these species, the researchers considered the smaller Lineated Woodpecker and Helmeted Woodpecker as subordinate mimics of the dominant Robust Woodpecker. According to the “interspecific social dominance hypothesis”, the three species should be ecological competitors and thus occupy in the same niches.

However, careful observations revealed clear niche differentiation. It turned out that the three species forage on different parts of the tree. Helmeted Woodpecker collected food on smaller trees and was often seen on dead branches in living trees. Lineated Woodpecker foraged on similar trees compared to Helmeted Woodpecker, but mainly used living healthy trees. And Robust Woodpecker was mainly observed on larger trees and frequently visited dead parts of living and decaying trees. In addition, the researchers did not record any direct interactions between the three species.

From left to right: Robust Woodpecker (Campephilus robustus), Lineated Woodpecker (Dryocopus lineatus) and Helmeted Woodpecker (Celeus galeatus). From: Fernández et al. (2020) Journal of Ornithology.

Deception

These results do not support the “interspecific social dominance hypothesis”. It could be that interspecific interactions in the past have driven these woodpecker species into different niches. But there are alternative explanations. The subordinate species might mimic the dominant species to deceive predators. The larger Robust Woodpecker is not an easy prey for small raptors, such as Sparrowhawks (genus Accipiter). These birds of prey might think twice before attacking a woodpecker that looks like a Robust Woodpecker.

It is also possible that the Lineated Woodpecker and the Helmeted Woodpecker are deceiving members of their own species to avoid direct competition. From a distance, birds might think that a dominant Robust Woodpecker is chiseling away at a tree branch and decide to look for another foraging spot. These explanations remain to be tested with more observations. I won’t mind putting my “All the Birds of the World” book aside and venturing into the Argentine forests.

References

Fernández, J. M., Areta, J. I., & Lammertink, M. (2020). Does foraging competition drive plumage convergence in three look-alike Atlantic Forest woodpecker species?. Journal of Ornithology, 161(4), 1105-1116.

Featured image; Lineated Woodpecker (Dryocopus lineatus) © panza-rayada | Wikimedia Commons